Advertisement

Tropical Plant Pathology

, Volume 43, Issue 3, pp 218–229 | Cite as

The influence of lulo (Solanum quitoense Lam) fruit maturity stage on polygalacturonase and pectate lyase secretion by Colletotrichum acutatum

  • Ana Patricia Martínez-González
  • Blanca Ligia Higuera-Mancipe
  • Sixta Tulia Martínez-Peralta
Original Article

Abstract

The influence of the lulo fruit maturity stage on the secretion of polygalacturonase (PG) and pectate lyase (PL) enzymes by Colletotrichum acutatum was determined. The study was performed using in vitro assays in the presence of exocarp and cell walls (CW) of the fruit at three different ripening stages (unripe, semi-ripe and ripe). The results showed that PG behaves as a constitutive enzyme and is only induced by semi-ripe CW, while PL is induced with the exocarp of lulo fruits at the three maturation stages, although its activity was highest with semi-ripe fruit. This enzymatic behavior might be related to the quiescent stage of the pathogen in the fruit, as C. acutatum remains quiescent until maturation begins. The profiles of PL induction were different in the presence of the CW and the exocarp inducers, whereas PG levels barely varied, indicating that the process of obtaining the CWs may eliminate a compound that contributes to the induction of PL secretion.

Keywords

Colletotrichum acutatum Solanum quitoense Lam fruit cell wall fruit exocarp hydrolytic enzymes pectinases 

Notes

Acknowledgements

This research was supported by DIB, Universidad Nacional de Colombia, 8003173, Quipu 201010010541.

References

  1. Agudelo-Romero P, Erban A, Rego C, Carbonell-Bejerano P, Nascimento T, Sousa L, Martínez-Zapater JM, Kopka J, Fortes AM (2015) Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea. Journal of Experimental Botany 66:1769–1785CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akimitsu K, Isshiki A, Ohtani K, Yamamoto H, Eshel D, Prusky D (2004) Sugars and pH: a clue to the regulation of fungal cell wall-degrading enzymes in plants. Physiological and Molecular Plant Pathology 65:271–275CrossRefGoogle Scholar
  3. Aleandri MP, Magro P, Chilosi G (2007) Modulation of host pH during the wheat-Fusarium culmorum interaction and its influence on the production and activity of pectolytic enzymes. Plant Pathology 56:517–525CrossRefGoogle Scholar
  4. Alkan N, Fortes AM (2015) Insights into molecular and metabolic events associated with fruit response to post-harvest fungal pathogens. Frontiers in Plant Science 6:889CrossRefPubMedPubMedCentralGoogle Scholar
  5. Alkan N, Fluhr R, Sherman A, Prusky D (2008) Role of ammonia secretion and pH modulation on pathogenicity of Colletotrichum coccodes on tomato fruit. Molecular Plant-Microbe Interactions 21:1058–1066CrossRefPubMedGoogle Scholar
  6. Alkan N, Davydov O, Sagi M, Fluhr R, Prusky D (2009) Ammonium secretion by Colletotrichum coccodes activates host NADPH oxidase activity enhancing host cell death and fungal virulence in tomato fruits. Molecular Plant-Microbe Interactions 22:1484–1491CrossRefPubMedGoogle Scholar
  7. Baroncelli R, Talhinhas P, Pensec F, Sukno SA, Le Floch G, Thon MR (2017) The Colletotrichum acutatum species complex as a model system to study evolution and host specialization in plant pathogens. Frontiers in Microbiology 8:2001CrossRefPubMedPubMedCentralGoogle Scholar
  8. Barras F, Van Gijsegem F, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annual Review of Phytopathology 32:201–234CrossRefGoogle Scholar
  9. Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Frontiers in Plant Science 5:1–8CrossRefGoogle Scholar
  10. Blanco-Ulate B, Morales-Cruz A, Amrine KC, Labavitch JM, Powell AL, Cantu D (2014) Genome-wide transcriptional profiling of Botrytis cinerea genes targeting plant cell walls during infections of different hosts. Frontiers in Plant Science 5:435CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brühlmann F (1995) Production and characterization of an extracellular pectate lyase from an Amycolata sp. Applied and Environmental Microbiology 61:3580–3585PubMedPubMedCentralGoogle Scholar
  12. Bugbee WM (1990) Purification and characteristics of pectin lyase from Rhizoctonia solani. Physiological and Molecular Plant Pathology 36:15–25CrossRefGoogle Scholar
  13. Caicedo O, Higuera BL (2007) Inducción de polifenoloxidasa en frutos de lulo (Solanum quitoense) como respuesta a la infección con Colletotrichum acutatum. Acta Biológica Colombiana 12:41–54Google Scholar
  14. Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum: current status and future directions. Studies in Mycology 73:181–213CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cantu D, Vicente AR, Greve LC, Dewey FM, Bennett AB, Labavitch JM, Powell ALT (2008a) The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proceedings of the National Academy of Sciences, USA 105:859–864CrossRefGoogle Scholar
  16. Cantu D, Vicente AR, Labavitch JM, Bennett AB, Powell AL (2008b) Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends in Plant Science 13:610–617CrossRefPubMedGoogle Scholar
  17. Cerón GS (2005) Detección de Colletotrichum (Penz) Sacc en estructuras vegetativas y reproductivas de Lulo Solanum quitoense Lam. M.Sc. Thesis. Universidad Nacional de Colombia, BogotáGoogle Scholar
  18. Collmer A, Ried JL, Mount MS (1988) Assay methods for pectic enzymes. Methods in Enzymology 161:329–335CrossRefGoogle Scholar
  19. Crawford MS, Kolattukudy PE (1987) Pectate lyase from Fusarium solani f. sp. pisi: purification, characterization, in vitro translation of the mRNA, and involvement in pathogenicity. Archives of Biochemistry and Biophysics 258:196–205CrossRefPubMedGoogle Scholar
  20. De Costa DM, Chandima AAG (2014) Effect of exogenous pH on development and growth of Colletotrichum musae and development of anthracnose in different banana cultivars in Sri Lanka. Journal of the National Science Foundation of Sri Lanka 42:229–240CrossRefGoogle Scholar
  21. De Lorenzo G, Ferrari S (2002) Polyalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Current Opinion in Plant Biology 5:1–5CrossRefGoogle Scholar
  22. De Silva DD, Crous PW, Ades PK, Hyde KD, Taylor PW (2017) Life styles of Colletotrichum species and implications for plant biosecurity. Fungal Biology Reviews 31:155–168CrossRefGoogle Scholar
  23. Diéguez-Uribeondo J, Förster H, Adaskaveg JE (2008) Visualization of localized pathogen-induced pH modulation in almond tissues infected by Colletotrichum acutatum using confocal scanning laser microscopy. Phytopathology 98:1171–1178CrossRefPubMedGoogle Scholar
  24. Drori N, Kramer-Haimovich H, Rollins J, Dinoor A, Okon Y, Pines O, Prusky D (2003) External pH and nitrogen source affect secretion of pectate lyase by Colletotrichum gloeosporioides. Applied and Environmental Microbiology 69:3258–3262CrossRefPubMedPubMedCentralGoogle Scholar
  25. Dubey AK, Yadav S, Kumar M, An G, Yadav D (2016) Molecular biology of microbial pectate lyase: a review. British Biotechnology Journal 13:1–26CrossRefGoogle Scholar
  26. Eshel D, Lichter A, Dinoor A, Prusky D (2002) Characterization of Alternaria alternata glucanase genes expressed during infection of resistant and susceptible persimmon fruits. Molecular Plant Pathology 3:347–358CrossRefPubMedGoogle Scholar
  27. Fernández-Acero FJ, Colby T, Harzen A, Carbú M, Wieneke U, Cantoral JM, Schmidt J (2010) 2-DE proteomic approach to the Botrytis cinerea secretome induced with different carbon sources and plant-based elicitors. Proteomics 10:2270–2280CrossRefPubMedGoogle Scholar
  28. Fisk CL, McDaniel MR, Strik BC, Zhao Y (2006) Physicochemical, sensory, and nutritive qualities of hardy kiwifruit (Actinidia arguta) ‘Ananasnaya’ as affected by harvest maturity and storage. Journal of Food Science 71:S204–S210CrossRefGoogle Scholar
  29. Forero DP, Carriazo JG, Osorio C (2016) Effect of different drying methods on morphological, thermal, and biofunctional properties of lulo (Solanum quitoense Lam.) fruit powders. Drying Technology 34:1085–1094CrossRefGoogle Scholar
  30. Fraissinet-Tachet L, Reymond-Cotton P, Fèvre M (1995) Characterization of a multigene family encoding an endopolygalacturonase in Sclerotinia sclerotiorum. Current Genetics 29:96–99CrossRefPubMedGoogle Scholar
  31. Gan P, Narusaka M, Kumakura N, Tsushima A, Takano Y, Narusaka Y, Shirasu K (2016) Genus-wide comparative genome analyses of Colletotrichum species reveal specific gene family losses and gains adaptation to specific infection lifestyles. Genome Biology and Evolution 8:1467–1481CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gómez M, Lajolo F, Cordenunsi B (2002) Evolution of soluble sugars during ripening of papaya fruit and its relation to sweet taste. Journal of Food Science 67:442–447CrossRefGoogle Scholar
  33. Gómez-García L, Martínez ST (2005) Induction of two pectolitic enzymes during the model Fusarium oxysporum f.sp. Dianthi-carnation. Revista Colombiana de Química 34:25–34Google Scholar
  34. González Loaiza DI, Ordóñez Santos LE, Vanegas Mahecha P, Vásquez Amariles HD (2014) Changes in physicochemical properties of the fruit of lulo (Solanum quitoense Lam.) harvested at three degrees of maturity. Acta Agronómica 63:11–17CrossRefGoogle Scholar
  35. Goulao LF, Santos J, de Sousa I, Oliveira CM (2007) Patterns of enzymatic activity of cell wall-modifying enzymes during growth and ripening of apples. Postharvest Biology and Technology 43:307–318CrossRefGoogle Scholar
  36. Guidarelli M, Carbone F, Mourgues F, Perrotta G, Rosati C, Bertolini P, Baraldi E (2011) Colletotrichum acutatum interactions with unripe and ripe strawberry fruits and differential responses at histological and transcriptional levels. Plant Pathology 60:685–697CrossRefGoogle Scholar
  37. ten Have A, Breuil WO, Wubben JP, Visser J, van Kan JA (2001) Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues. Fungal Genetics and Biology 33:97–105CrossRefPubMedGoogle Scholar
  38. Hunter RE (1974) Inactivation of pectic enzymes by polyphenols in cotton seedlings of different ages infected with Rhizoctonia solani. Physiological Plant Pathology 4:151–159CrossRefGoogle Scholar
  39. Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Molecular Plant-Microbe Interactions 14:749–757CrossRefPubMedGoogle Scholar
  40. Jayani RS, Saxena S, Gupta R (2005) Microbial pectinolytic enzymes: a review. Process Biochemistry 40:2931–2944CrossRefGoogle Scholar
  41. Jones TM, Anderson AJ, Albersheim P (1972) Host-pathogen interactions. Physiological Plant Pathology 2:153–166CrossRefGoogle Scholar
  42. Jurick WM, Janisiewicz WJ, Saftner RA, Vico I, Gaskins VL, Park E, Forsline P, Fazio G, Conway WS (2011) Identification of wild apple germplasm (Malus spp.) accessions with resistance to the postharvest decay pathogens Penicillium expansum and Colletotrichum acutatum. Plant Breeding 130:481–486CrossRefGoogle Scholar
  43. Kramer-Haimovich H, Servi E, Katan T, Rollins J, Okon Y, Prusky D (2006) Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion and fruit pathogenicity. Applied and Environmental Microbiology 72:1034–1039CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall-degrading enzymes and their secretion in plant pathogenic fungi. Annual Review of Phytopathology 52:427–451CrossRefPubMedGoogle Scholar
  45. Lara-Márquez A, Oyama K, Zavala-Páramo MG, Villa-Rivera MG, Conejo-Saucedo U, Cano-Camacho H (2017) Evolutionary analysis of pectin lyases of the genus Colletotrichum. Journal of Molecular Evolution 85:120–136CrossRefPubMedGoogle Scholar
  46. Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S, Kahmann R (2015) Fungal effectors and plant susceptibility. Annual Review of Plant Biology 66:513–545CrossRefPubMedGoogle Scholar
  47. Lyu X, Shen C, Fu Y, Xie J, Jiang D, Li G, Cheng J (2015) Comparative genomic and transcriptional analyses of the carbohydrate-active enzymes and secretomes of phytopathogenic fungi reveal their significant roles during infection and development. Scientific Reports 5:15565CrossRefPubMedPubMedCentralGoogle Scholar
  48. Manteau S, Abouna S, Lambert B, Legendre L (2003) Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. FEMS Microbiology Ecology 43:359–366CrossRefPubMedGoogle Scholar
  49. Marín-Rodríguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. Journal of Experimental Botany 53:2115–2119CrossRefPubMedGoogle Scholar
  50. Martínez ST, Martínez P, González VC, Higuera BL (2012) Determinación in vitro de los patrones de inducción de una endoxilanasa (EC 3.2.1.8) secretada por Fusarium oxysporum f. sp. dianthi. Purificación y caracterización parcial. Revista Colombiana de Química 41:359–376Google Scholar
  51. Mejía CM, Gaviria DA, Duque AL, Rengifo RM, Aguilar EF, Hernán AA (2012) Physicochemical characterization of the lulo (Solanum quitoense Lam.) castilla variety in six ripening stages. Vitae 19:157–165Google Scholar
  52. Mengiste T (2012) Plant immunity to necrotrophs. Annual Review of Phytopathology 50:267–294CrossRefPubMedGoogle Scholar
  53. Miles TD, Day B, Schilder AC (2011) Identification of differentially expressed genes in a resistant versus a susceptible blueberry cultivar after infection by Colletotrichum acutatum. Molecular Plant Pathology 12:463–477CrossRefPubMedGoogle Scholar
  54. Miles TD, Hancock JF, Callow P, Schilder AMC (2012) Evaluation of screening methods and fruit composition in relation to anthracnose fruit rot resistance in blueberries. Plant Pathology 61:555–566CrossRefGoogle Scholar
  55. Miyara I, Shafran H, Haimovich HK, Rollins J, Sherman A, Prusky D (2008) Multi-factor regulation of pectate lyase secretion by Colletotrichum gloeosporioides pathogenic on avocado fruits. Molecular Plant Pathology 9:281–291CrossRefPubMedGoogle Scholar
  56. Nelson N (1944) A photometric adaptation of the Somogyi method for determination of glucose. Journal of Biological Chemistry 153:378–380Google Scholar
  57. NTC 4592 (1999) Instituto Colombiano de Normas Técnicas. Productos de Frutas y Verduras. Determinación del pH. Icontec, BogotáGoogle Scholar
  58. NTC 4623 (1999) Instituto Colombiano de Normas Técnicas. Productos de Frutas y Verduras. Determinación de la acidez titulable. Icontec, BogotáGoogle Scholar
  59. NTC 4624 (1999) Instituto Colombiano de Normas Técnicas. Jugos de Frutas y Hortalizas. Determinación del contenido de sólidos solubles. Método refractométrico. Icontec, BogotáGoogle Scholar
  60. Ochoa J, Clements C, Barrera V, Dominguez JM, Ellis MA, Alwang J (2016) IPM packages for naranjilla: sustainable production in an environmentally fragile region. In: Muniappan R, Heinrichs EA (eds) Integrated pest management of tropical vegetable crops. Springer Netherlands, Amsterdam, pp 209–221CrossRefGoogle Scholar
  61. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmüller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun M-H, Lee Y-H, Miyara I, Moore N, Neumann U, Nordström K, Panaccione DG, Panstruga R, Place M, Proctor RH, Prusky D, Rech G, Reinhardt R, Rollins JA, Rounsley S, Schardl CL, Schwartz DC, Shenoy N, Shirasu K, Sikhakolli UR, Stüber K, Sukno SA, Sweigard JA, Takano Y, Takahara H, Trail F, van der Does HC, Voll LM, Will I, Young S, Zeng Q, Zhang J, Zhou S, Dickman MB, Schulze-Lefert P, Ver Loren van Themaat E, Ma L-J, Vaillancourt LJ (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics 44:1060–1065CrossRefPubMedGoogle Scholar
  62. Perfect SE, Hughes HB, O'Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal-plant interactions. Fungal Genetics and Biology 27:186–198CrossRefPubMedGoogle Scholar
  63. Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena an overview. Critical Reviews in Food Science and Nutrition 47:19CrossRefGoogle Scholar
  64. Prusky D, Lichter A (2008) Mechanisms modulating fungal attack in post-harvest pathogen interactions and their control. European Journal of Plant Pathology 121:281–289CrossRefGoogle Scholar
  65. Prusky D, Yakoby N (2003) Pathogenic fungi: leading or led by ambient pH ? Molecular Plant Pathology 4:509–516CrossRefPubMedGoogle Scholar
  66. Prusky D, Kobiler I, Yakoby B (1988) Involvement of epicatechin in cultivar susceptibility of avocado fruits to Colletotrichum gloeosporioides after harvest. Phytopathology 123:140–146CrossRefGoogle Scholar
  67. Prusky D, McEvoy JL, Leverentz B, Conway WS (2001) Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Molecular Plant-Microbe Interactions 14:1105–1113CrossRefPubMedGoogle Scholar
  68. Prusky D, Alkan N, Mengiste T, Fluhr R (2013) Quiescent and necrotrophic lifestyle choise during postharvest disease. Annual Review of Phytopathology 51:155–176CrossRefPubMedGoogle Scholar
  69. Prusky D, Barad S, Ment D, Bi F (2016) The pH modulation by fungal secreted molecules: a mechanism affecting pathogenicity by postharvest pathogens. Israel Journal of Plant Sciences 63:22–30CrossRefGoogle Scholar
  70. Ramos AM, Gally M, García MC, Levin L (2010) Pectinolytic enzyme production by Colletotrichum truncatum, causal agent of soybean anthracnose. Revista Iberoamericana de Micología 27:186–190CrossRefPubMedGoogle Scholar
  71. Ramos AM, Gally M, Szapiro G, Itzcovich T, Carabajal M, Levin L (2016) In vitro growth and cell wall degrading enzyme production by Argentinean isolates of Macrophomina phaseolina, the causative agent of charcoal rot in corn. Revista Argentina de Microbiología 48:267–273CrossRefPubMedGoogle Scholar
  72. Reignault P, Valette-Collet O, Boccara M (2008) The importance of fungal pectinolytic enzymes in plant invasion, host adaptability and symptom type. European Journal of Plant Pathology 120:1–11CrossRefGoogle Scholar
  73. Rodríguez JM, Restrepo LP (2011) Activity of pectic enzymes involved in the ripening process of lulo (Solanum quitoense Lam.) Agronomía Colombiana 29:63–71Google Scholar
  74. Rogers LM, Kim Y, Guo W, Gonzales-Candelas L, Li D, Kolattukudy PE (2000) Requirement of either a host- or pectin- induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proceedings of the National Academy of Sciences, USA 97:9813–9818CrossRefGoogle Scholar
  75. Roncero MI, Di Pietro A, Ruiz-Roldán MC, Huertas-González MD, Garcia-Maceira FI, Méglecz E, Jiménez A, Caracuel Z, Sancho-Zapatero R, Hera C, Gomez-Gomez E, Ruiz-Rubio M, Cl G-V, Páez MJ (2000) Role of cell wall-degrading enzymes in pathogenicity of Fusarium oxysporum. Revista Iberoamericana de Micología 17:S47–S53PubMedGoogle Scholar
  76. de Sain M, Rep M (2015) The role of pathogen-secreted proteins in fungal vascular wilt diseases. International Journal of Molecular Sciences 16:23970–23993CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sezer A, Dolar FS (2012) Colletotrichum acutatum, a new pathogen of hazelnut. Journal of Phytopathology 160:428–430CrossRefGoogle Scholar
  78. Shah P, Powell ALT, Orlando R, Bergmann C, Gutierrez-Sanchez G (2012) Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea. Journal of Proteome Research 11:2178–2192CrossRefPubMedPubMedCentralGoogle Scholar
  79. Sharma M, Kuishrestha S (2015) Colletotrichum gloeosporioides: an anthracnose causing pathogen of fruits and vegetables. Biosciences, Biotechnology Research Asia 12:1233–1246CrossRefGoogle Scholar
  80. Sherwood RT (1966) Pectin lyase and polygalacturonase production by Rhizoctonia solani and other fungi. Phytopathology 56:279–286CrossRefGoogle Scholar
  81. Shih J, Wei Y, Goodwin P (2000) A comparison of the pectate lyase genes, pel-1 and pel-2, of Colletotrichum gloeosporioides f. sp. malvae and the relationship between their expression in culture and during necrotrophic infection. Gene 243:139–150CrossRefPubMedGoogle Scholar
  82. Somogyi M (1952) Notes on sugar determination. Journal of Biological Chemistry 195:19–23Google Scholar
  83. Talhinhas P, Mota-Capitão C, Martins S, Ramos AP, Neves-Martins J, Guerra-Guimarães L, Várzea V, Silva MC, Sreenivasaprasad S, Oliveira H (2011) Epidemiology, histopathology and aetiology of olive anthracnose caused by Colletotrichum acutatum and C. gloeosporioides in Portugal. Plant Pathology 60:483–495CrossRefGoogle Scholar
  84. Thrower LB (1966) Terminology for plant parasites. Journal of Phytopathology 56:258–259CrossRefGoogle Scholar
  85. Timmer LW, Peres NA (2015) Where have all the flowers gone? Postbloom fruit drop of citrus in the Americas. Journal of Citrus Pathology 2:1–6Google Scholar
  86. Underwood W (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Frontiers in Plant Science 3:85CrossRefPubMedPubMedCentralGoogle Scholar
  87. Van der Cruyssen G, de Meester E, Kamoen O (1994) Expression of polygalacturonase of Botrytis cinerea in vitro and in vivo. Mededelingen-Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent 59:895–905Google Scholar
  88. Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends in Plant Science 9:203–209CrossRefPubMedGoogle Scholar
  89. Walton JD (1994) Deconstructing the wall cell. Plant Physiology 104:1113–1118CrossRefPubMedPubMedCentralGoogle Scholar
  90. Wattad C, Dinoor A, Prusky D (1994) Purification of pectate lyase produced by Colletotrichum gloeosporioides and its inhibition by epicatechin: a possible factor involved in the resistance of unripe avocado fruits to anthracnose. Molecular Plant-Microbe Interactions 7:293–297CrossRefPubMedGoogle Scholar
  91. Wei YD, Byer KN, Goodwin PH (1997) Hemibiotrophic infection of round-leaved mallow by Colletotrichum gloeosporioides f. sp. malvae in relation to leaf senescence and reducing reagents. Mycological Research 101:357–364CrossRefGoogle Scholar
  92. Wharton PS, Diéguez-Uribeondo J (2004) The biology or Colletotrichum acutatum. Anales del Jardin Botánico de Madrid 61:3–22Google Scholar
  93. Wubben JP, Mulder W, ten Have A, Van Kan JAL, Visser J (1999) Cloning and partial characterization of endopolygalacturonase genes from Botrytis cinerea. Applied and Environmental Microbiology 65:1596–1602PubMedPubMedCentralGoogle Scholar
  94. Wubben JP, ten Have A, van Kan JAL, Visser J (2000) Regulation of endopolygalacturonase gene expression in Botrytis cinerea by galacturonic acid, ambient pH and carbon catabolite repression. Current Genetics 37:152–157CrossRefPubMedGoogle Scholar
  95. Yadav S, Yadav PK, Yadav D, Yadav KDS (2009) Pectin lyase: a review. Process Biochemistry 44:1–10CrossRefGoogle Scholar
  96. Yakoby N, Kobilier I, Dinoor A, Prusky D (2000) pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Applied and Environmental Microbiology 66:1026–1030CrossRefPubMedPubMedCentralGoogle Scholar
  97. Yakoby N, Beno-Moualem D, Keen N, Dinoor A, Pines O, Prusky D (2001) Colletotrichum gloeosporioides pelB is an important virulence factor in avocado fruit-fungus interaction. Molecular Plant-Microbe Interactions 14:988–995CrossRefPubMedGoogle Scholar
  98. Yarullina LG, Akhatova AR, Kasimova RI (2016) Hydrolytic enzymes and their proteinaceous inhibitors in regulation of plant–pathogen interactions. Russian Journal of Plant Physiology 63:193–203CrossRefGoogle Scholar
  99. Zhang J, Bruton BD, Biles CL (2014) Cell wall-degrading enzymes of Didymella bryoniae in relation to fungal growth and virulence in cantaloupe fruit. European Journal of Plant Pathology 139:749–761CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2018

Authors and Affiliations

  • Ana Patricia Martínez-González
    • 1
  • Blanca Ligia Higuera-Mancipe
    • 1
  • Sixta Tulia Martínez-Peralta
    • 1
  1. 1.Department of ChemistryUniversidad Nacional de Colombia (Bogotá campus)BogotáColombia

Personalised recommendations